Microbial Community Stratification Linked to Utilization of Carbohydrates and Phosphorus Limitation in a Boreal Peatland at Marcell Experimental Forest, Minnesota, USA

Abstract

e This study investigated the abundance, distribution, and composition of microbial communities at the watershed scale in a boreal peatland within the Marcell Experimental Forest (MEF), Minnesota, USA. Through a close coupling of next-generation sequencing, biogeochemistry, and advanced analytical chemistry, a biogeochemical hot spot was revealed in the mesotelm (30-to 50-cm depth) as a pronounced shift in microbial community composition in parallel with elevated peat decomposition. The relative abundance of Acidobacteria and the Syntrophobacteraceae, including known hydrocarbon-utilizing genera, was positively correlated with carbohydrate and organic acid content, showing a maximum in the mesotelm. The abundance of Archaea (primarily crenarchaeal groups 1.1c and 1.3) increased with depth, reaching up to 60% of total small-subunit (SSU) rRNA gene sequences in the deep peat below the 75-cm depth. Stable isotope geochemistry and potential rates of methane production paralleled vertical changes in methanogen community composition to indicate a predominance of acetoclastic methanogenesis mediated by the Methanosarcinales in the mesotelm, while hydrogen-utilizing methanogens predominated in the deeper catotelm. RNA-derived pyrosequence libraries corroborated DNA sequence data to indicate that the above-mentioned microbial groups are metabolically active in the mid-depth zone. Fungi showed a maximum in rRNA gene abundance above the 30-cm depth, which comprised only an average of 0.1% of total bacterial and archaeal rRNA gene abundance, indicating prokaryotic dominance. Ratios of C to P enzyme activities approached 0.5 at the acrotelm and catotelm, indicating phosphorus limitation. In contrast, P limitation pressure appeared to be relieved in the mesotelm, likely due to P solubilization by microbial production of organic acids and C-P lyases. Based on path analysis and the modeling of community spatial turnover, we hypothesize that P limitation outweighs N limitation at MEF, and microbial communities are structured by the dominant shrub, Chamaedaphne calyculata, which may act as a carbon source for major consumers in the peatland.

Alpha- and Gammaproteobacterial Methanotrophs Codominate the Active Methane-Oxidizing Communities in an Acidic Boreal Peat Bog

“…However, more recently, a number of type II methanotrophs (Methylocella, Methylocapsa, and Methylocystis) have been characterized as facultative methanotrophs capable of conserving energy for growth on multicarbon compounds such as acetate, pyruvate, succinate, malate, and ethanol (12). Although members of the phylum Verrucomicrobia have been widely detected in peatlands, none has been definitively linked to methanotrophy, and thus more research is needed to ascertain the role of Verrucomicrobia in the carbon cycle of peatlands (8,13,14,15,16).Aerobic methane oxidation in proteobacterial methanotrophs is catalyzed by the enzyme methane monooxygenase (MMO), either particulate MMO (pMMO) or a soluble MMO (sMMO). The genes pmoA (encoding the 27-kDa subunit of pMMO) and mmoX (encoding the alpha-subunit of the hydroxylase of sMMO) as well as 16S rRNA genes have been used most often as molecular markers to characterize methanotrophs in peatlands and other environments (6,17,18,19,20,21,22,23).…”

“…However, more recently, a number of type II methanotrophs (Methylocella, Methylocapsa, and Methylocystis) have been characterized as facultative methanotrophs capable of conserving energy for growth on multicarbon compounds such as acetate, pyruvate, succinate, malate, and ethanol (12). Although members of the phylum Verrucomicrobia have been widely detected in peatlands, none has been definitively linked to methanotrophy, and thus more research is needed to ascertain the role of Verrucomicrobia in the carbon cycle of peatlands (8,13,14,15,16).…”

Metabolic potential of fatty acid oxidation and anaerobic respiration by abundant members of Thaumarchaeota and Thermoplasmata in deep anoxic peat

“…The ISME Journal (2015Journal ( ) 9, 2740Journal ( -2744doi:10.1038/ismej.2015published online 22 May 2015 Peatlands represent carbon rich environments shown to sequester approximately one-third of all soil carbon on Earth (Gorham, 1991). Archaea are particularly abundant in peat soils, with Crenarchaea and Thaumarchaeota comprising up to 60% of the microbial community in subsurface peats (Kemnitz et al, 2007;Lin et al, 2012;Basiliko et al, 2013;Hawkins et al, 2014;Lin et al, 2014). Thaumarchaeotal groups 1.1b and 1.1c were recently estimated to account for 76 ± 33% of total archaea in global soil samples (Auguet et al, 2010), suggesting they may have key roles in Earth's biogeochemical cycles.…”

“…LCFA oxidation is thermodynamically impossible without coupling to respiration activity or the consumption of reducing equivalents (hydrogen/formate) (Schink, 1997). Considering the lack of genes related to sulfate/nitrate reduction in Fn1 and occurrence of abundant hydrogenotrophic methanogens in the deep peat (Lin et al, 2014), it is possible that Fn1 establishes a syntrophic interaction with methanogens and/or uses fumarate as a TEA to degrade LCFA. In addition, we reason that Thermoplasmata Bg1 may couple sulfite (and potentially sulfonate) reduction to LCFA oxidation, and organosulfonate is abundant in peat soils and humic substances (Autry and Fitzgerald, 1990) relative to the low levels of inorganic sulfate observed in peats.…”

Next-Generation Pyrosequencing Analysis of Microbial Biofilm Communities on Granular Activated Carbon in Treatment of Oil Sands Process-Affected Water

“…Among the other phyla, the members of Acidobacteria play an important role in the degradation of carbohydrates in boreal forest peat land, as these microbial groups are abundant in RNAderived sequence libraries and culture studies indicate that they are well adapted to acidic, nutrient-poor conditions (49). Nitrospirae are involved in denitrification, sulfur oxidation, and sulfate reduction, showing their considerable capacity for adaptation to variable geochemical conditions and roles in local biogeochemical cycles (50).…”